Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant

1. Time and energy are key currencies in animal ecology, and judicious management of these is a primary focus for natural selection. At present, however, there are only two main methods for estimation of rate of energy expenditure in the field, heart rate and doubly labelled water, both of which have been used with success; but both also have their limitations. 2. The deployment of data loggers that measure acceleration is emerging as a powerful tool for quantifying the behaviour of free-living animals. Given that animal movement requires the use of energy, the accelerometry technique potentially has application in the quantification of rate of energy expenditure during activity. 3. In the present study, we test the hypothesis that acceleration can serve as a proxy for rate of energy expenditure in free-living animals. We measured rate of energy expenditure as rates of O2 consumption (VO2) and CO2 production (VCO2) in great cormorants (Phalacrocorax carbo) at rest and during pedestrian exercise. VO2 and VCO2 were then related to overall dynamic body acceleration (ODBA) measured with an externally attached three-axis accelerometer. 4. Both VO2 and VCO2 were significantly positively associated with ODBA in great cormorants. This suggests that accelerometric measurements of ODBA can be used to estimate VO2 and VCO2 and, with some additional assumptions regarding metabolic substrate use and the energy equivalence of O2 and CO2, that ODBA can be used to estimate the activity specific rate of energy expenditure of free-living cormorants. 5. To verify that the approach identifies expected trends in from situations with variable power requirements, we measured ODBA in free-living imperial cormorants (Phalacrocorax atriceps) during foraging trips. We compared ODBA during return and outward foraging flights, when birds are expected to be laden and not laden with captured fish, respectively. We also examined changes in ODBA during the descent phase of diving, when power requirements are predicted to decrease with depth due to changes in buoyancy associated with compression of plumage and respiratory air. 6. In free-living imperial cormorants, ODBA, and hence estimated VO2, was higher during the return flight of a foraging bout, and decreased with depth during the descent phase of a dive, supporting the use of accelerometry for the determination of activity-specific rate of energy expenditure.     

Assessing the development and application of the accelerometry technique for estimating energy expenditure

A theoretically valid proxy of energy expenditure is the acceleration of an animal's mass due to the movement of its body parts. Acceleration can be measured by an accelerometer and recorded onto a data logging device. Relevant studies have usually derived a measure of acceleration from the raw data that represents acceleration purely due to movement of the animal. This is termed ‘overall dynamic body acceleration’ (ODBA) and to date has proved a robust derivation of acceleration for use as an energy expenditure proxy. Acceleration data loggers are generally easy to deploy and the measures recorded appear robust to slight variation in location and orientation. This review discusses important issues concerning the accelerometry technique for estimating energy expenditure and ODBA; deriving ODBA, calibrating ODBA, acceleration logger recording frequencies, scenarios where ODBA is less likely to be valid, and the power in recording acceleration and heart rate together. While present evidence suggests that ODBA may not quantify energy expenditure during diving by birds and mammals, several recent studies have assessed changes in mechanical work in such species qualitatively through variation in ODBA during periods of submergence. The use of ODBA in field metabolic studies is likely to continue growing, supported by its relative ease of use and range of applications.     

Application of Overall Dynamic Body Acceleration as a Proxy for Estimating the Energy Expenditure of Grazing Farm Animals: Relationship with Heart Rate

Estimating the energy expenditure of farm animals at pasture is important for efficient animal management. In recent years, an alternative technique for estimating energy expenditure by measuring body acceleration has been widely performed in wildlife and human studies, but the availability of the technique in farm animals has not yet been examined. In the present study, we tested the potential use of an acceleration index, overall dynamic body acceleration (ODBA), as a new proxy for estimating the energy expenditure of grazing farm animals (cattle, goats and sheep) at pasture with the simultaneous evaluation of a conventional proxy, heart rate. Body accelerations in three axes and heart rate for cows (n = 8, two breeds), goats (n = 6) and sheep (n = 5) were recorded, and the effect of ODBA calculated from the body accelerations on heart rate was analyzed. In addition, the effects of the two other activity indices, the number of steps and vectorial dynamic body acceleration (VeDBA), on heart rate were also investigated. The results of the comparison among three activity indices indicated that ODBA was the best predictor for heart rate. Although the relationship between ODBA and heart rate was different between the groups of species and breeds and between individuals (P<0.01), the difference could be explained by different body weights; a common equation could be established by correcting the body weights (M: kg): heart rate (beats/min) = 147.263∙M ^-0.141 + 889.640∙M ^-0.179∙ODBA (g). Combining this equation with the previously reported energy expenditure per heartbeat, we estimated the energy expenditure of the tested animals, and the results indicated that ODBA is a good proxy for estimating the energy expenditure of grazing farm animals across species and breeds. The utility and simplicity of the procedure with acceleration loggers could make the accelerometry technique a worthwhile option in field research and commercial farm use.     

Acceleration Data Reveal Highly Individually Structured Energetic Landscapes in Free-Ranging Fishers (Pekania pennanti)

Investigating animal energy expenditure across space and time may provide more detailed insight into how animals interact with their environment. This insight should improve our understanding of how changes in the environment affect animal energy budgets and is particularly relevant for animals living near or within human altered environments where habitat change can occur rapidly. We modeled fisher (Pekania pennanti) energy expenditure within their home ranges and investigated the potential environmental and spatial drivers of the predicted spatial patterns. As a proxy for energy expenditure we used overall dynamic body acceleration (ODBA) that we quantified from tri-axial accelerometer data during the active phases of 12 individuals. We used a generalized additive model (GAM) to investigate the spatial distribution of ODBA by associating the acceleration data to the animals'' GPS-recorded locations. We related the spatial patterns of ODBA to the utilization distributions and habitat suitability estimates across individuals. The ODBA of fishers appears highly structured in space and was related to individual utilization distribution and habitat suitability estimates. However, we were not able to predict ODBA using the environmental data we selected. Our results suggest an unexpected complexity in the space use of animals that was only captured partially by re-location data-based concepts of home range and habitat suitability. We suggest future studies recognize the limits of ODBA that arise from the fact that acceleration is often collected at much finer spatio-temporal scales than the environmental data and that ODBA lacks a behavioral correspondence. Overcoming these limits would improve the interpretation of energy expenditure in relation to the environment.     

Assessing the validity of the accelerometry technique for estimating the energy expenditure of diving double-crested cormorants Phalacrocorax auritus

Over the past few years, acceleration-data loggers have been used to provide calibrated proxies of energy expenditure: the accelerometry technique. Relationships between rate of oxygen consumption and a derivation of acceleration data termed "overall dynamic body acceleration" (ODBA) have now been generated for a range of species, including birds, mammals, and amphibians. In this study, we examine the utility of the accelerometry technique for estimating the energy expended by double-crested cormorants Phalacrocorax auritus to undertake a dive cycle (i.e., a dive and the subsequent pause at the surface before another dive). The results show that ODBA does not calibrate with energy expenditure in diving cormorants, where energy expenditure is calculated from measures of oxygen uptake during surface periods between dives. The possible explanations include reasons why energy expenditure may not relate to ODBA but also reasons why oxygen uptake between dives may not accurately represent energy expenditure during a dive cycle.     

Measuring energy expenditure in sub-adult and hatchling sea turtles via accelerometry

Measuring the metabolic of sea turtles is fundamental to understanding their ecology yet the presently available methods are limited. Accelerometry is a relatively new technique for estimating metabolic rate that has shown promise with a number of species but its utility with air-breathing divers is not yet established. The present study undertakes laboratory experiments to investigate whether rate of oxygen uptake ( o ₂) at the surface in active sub-adult green turtles Chelonia mydas and hatchling loggerhead turtles Caretta caretta correlates with overall dynamic body acceleration (ODBA), a derivative of acceleration used as a proxy for metabolic rate. Six green turtles (25–44 kg) and two loggerhead turtles (20 g) were instrumented with tri-axial acceleration logging devices and placed singly into a respirometry chamber. The green turtles were able to submerge freely within a 1.5 m deep tank and the loggerhead turtles were tethered in water 16 cm deep so that they swam at the surface. A significant prediction equation for mean o ₂ over an hour in a green turtle from measures of ODBA and mean flipper length (R² = 0.56) returned a mean estimate error across turtles of 8.0%. The range of temperatures used in the green turtle experiments (22–30°C) had only a small effect on o ₂. A o ₂-ODBA equation for the loggerhead hatchling data was also significant (R² = 0.67). Together these data indicate the potential of the accelerometry technique for estimating energy expenditure in sea turtles, which may have important applications in sea turtle diving ecology, and also in conservation such as assessing turtle survival times when trapped underwater in fishing nets.     

Behavioural flexibility allows an invasive vertebrate to survive in a semi-arid environment

Plasticity or evolution in behavioural responses are key attributes of successful animal invasions. In northern Australia, the invasive cane toad (Rhinella marina) recently invaded semi-arid regions. Here, cane toads endure repeated daily bouts of severe desiccation and thermal stress during the long dry season (April–October). We investigated whether cane toads have shifted their ancestral nocturnal rehydration behaviour to one that exploits water resources during the day. Such a shift in hydration behaviour could increase the fitness of individual toads by reducing exposure to desiccation and thermal stress suffered during the day even within terrestrial shelters. We used a novel method (acoustic tags) to monitor the daily hydration behaviour of 20 toads at two artificial reservoirs on Camfield station, Northern Territory. Remarkably, cane toads visited reservoirs to rehydrate during daylight hours, with peaks in activity between 9.00 and 17.00. This diurnal pattern of rehydration activity contrasts with nocturnal rehydration behaviour exhibited by adult toads in their native geographical range and more mesic parts of Australia. Our results demonstrate that cane toads phase shift a key behaviour to survive in a harsh semi-arid landscape. Behavioural phase shifts have rarely been reported in invasive species but could facilitate ongoing invasion success.     

The relationship between oxygen consumption and body acceleration in a range of species

The ability to measure the energy expenditure of free-ranging animals is of great importance but the techniques available each have their limitations. Recently, as an alternative to more established techniques, an integrated measure of body acceleration termed overall dynamic body acceleration (ODBA) has been used as a calibrated proxy for rate of oxygen consumption (V(O(2))) and hence metabolic rate. The present study tested the potential of this technique, firstly by expanding the range of species for which the V(O(2))-ODBA relationship has been defined and secondly by undertaking a validation exercise to explore the accuracy of predictions made using ODBA. V(O(2))-ODBA relationships during terrestrial locomotion were established for several bipedal and quadrupedal endotherms and compiled with similar relationships previously determined in other species. A model incorporating all of these species showed that ODBA is an excellent predictor of V(O(2)) but there is variation in the V(O(2))-ODBA relationship between species, and further variation within some species. Including measurements such as body mass and structural size in prediction equations might further improve the predictive power of the 'ODBA technique' and eliminate species-specific differences. In the validation exercise, estimate errors were calculated for the species-specific predictive equations. The use of ODBA to estimate V(O(2)) was valid across all species examined and may show a greater potential for estimating energy expenditure for individual animals than other techniques.     

The metabolic rates associated with resting, and with the performance of agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae)

We measured the metabolic rates as a direct estimate of energy expenditure of individual Neolamprologus pulcher, a cooperatively breeding cichlid fish, when resting and when performing agonistic, submissive or digging behaviours in a respirometer. Standard and routine metabolic rates increased linearly with body mass (range 0.9–8.4 g) when plotted on a doubly logarithmic scale (linear regression equations: standard metabolic rate: log individual oxygen consumption rate = 0.65 + 0.86 log body mass; routine metabolic rate: log individual oxygen consumption rate = 0.75 + 0.86 log body mass). Routine metabolic rates were, on average, 30% higher than standard metabolic rates. Submissive and agonistic behaviours raised routine metabolic rates by factors of 3.3 and 3.9, respectively. Digging resulted in a 6.1-fold increase of routine metabolic rates. Differences in metabolic rates between active and resting rates were statistically significant. However, those between the three behaviours were not. Mean opercular beat frequencies correlated significantly with routine metabolic rates and with metabolic rates when performing specific behaviours, which offers methodological prospects for field measurements. In N. pulcher, the high energy expenditure for submissive behaviour may indicate that this is a reliable signal. The considerable energy expenditure involved in territory defence suggests that these costs should be considered in addition to risk in cost-benefit analyses. This is the first study in which the energy expenditures of specific social and territory maintenance behaviours of individual fish were measured directly by respirometry and within the usual social setting of the fish. Accepted: 20 February 1998     

Cane Toads on Cowpats: Commercial Livestock Production Facilitates Toad Invasion in Tropical Australia

Habitat disturbance and the spread of invasive organisms are major threats to biodiversity, but the interactions between these two factors remain poorly understood in many systems. Grazing activities may facilitate the spread of invasive cane toads (Rhinella marina) through tropical Australia by providing year-round access to otherwise-seasonal resources. We quantified the cane toad’s use of cowpats (feces piles) in the field, and conducted experimental trials to assess the potential role of cowpats as sources of prey, water, and warmth for toads. Our field surveys show that cane toads are found on or near cowpats more often than expected by chance. Field-enclosure experiments show that cowpats facilitate toad feeding by providing access to dung beetles. Cowpats also offer moist surfaces that can reduce dehydration rates of toads and are warmer than other nearby substrates. Livestock grazing is the primary form of land use over vast areas of Australia, and pastoral activities may have contributed substantially to the cane toad’s successful invasion of that continent.     

Seasonal differences in energy expenditure,flight characteristics and spatial utilization of Dalmatian Pelicans Pelecanus crispus in Greece

Animals typically adjust their behaviour to their changing environment throughout the annual cycle, modulating key processes such as the timing of breeding and the onset of migration. Such behavioural changes are commonly manifested in the movements and the energetic balance of individuals in relation to their species‐specific physiological characteristics, habitat attributes and the environmental properties of their distribution ranges. We used GPS and acceleration data collected using transmitters on free‐ranging birds to quantify annual movement patterns and estimate energy expenditure of the Dalmatian Pelican Pelecanus crispus, a large, soaring avian species which performs short‐distance migration and spends its entire annual cycle in mid‐latitudes. To assess the representativeness of our results, the transmitter effect was also tested. We found that daily trends in the overall dynamic body acceleration (ODBA; a proxy for energy expenditure) differed among seasons, with the highest values occurring during spring and the lowest during winter. Long inter‐lake flights were very rare in winter, and the number of flights and ODBA during spring was higher than during summer, suggesting greater motivation to move in spring. Although transmitters may have affected the birds, as none of the tagged birds bred, we found seasonal differences in behaviour and activity level. The observed patterns in differences in activity levels, long‐distance flights and flight characteristics between seasons suggest an annual rhythm of energy expenditure. These findings allow a better understanding of bird phenology, specifically regarding adaptations to wintering in a cold climate by reducing movement‐driven energy expenditure. Finally, the identification of periods with high and low energy expenditure may guide future conservation efforts by adjusting conservation plans in accordance with changing needs during the annual cycle.     

Dynamic body acceleration increases by 20% during flight ontogeny of greylag geese Anser anser

Despite our knowledge of the biophysical and behavioural changes during flight ontogeny in juvenile birds, little is known about the changes in the mechanical aspects of energy expenditure during early flight development, particularly in migratory species. Here, we investigate in a unique experimental setup how energy expended during flights changes over time beginning with early ontogeny. We calculate overall dynamic body acceleration (ODBA) as a proxy for energy expenditure in a group of hand raised greylag geese Anser anser trained to fly behind a microlight aircraft. We propose two potential hypotheses; energy expenditure either increases with increasing physiological suitability (the ‘physical development hypothesis’), or decreases as a result of behavioural improvements mitigating flight costs (the ‘behavioural development hypothesis’). There was a significant temporal increase of flight duration and ODBA over time, supporting the ‘physical development hypothesis’. This suggests that early on in flight ontogeny behavioural development leading to flight efficiency plays a weaker role in shaping ODBA changes than the increased physical ability to expend energy in flight. We discuss these findings and the implications of flight development on the life history of migratory species.     

Personality,Metabolic Rate and Aerobic Capacity

Personality traits and cardiorespiratory fitness in older adults are reliable predictors of health and longevity. We examined the association between personality traits and energy expenditure at rest (basal metabolic rate) and during normal and maximal sustained walking. Personality traits and oxygen (VO₂) consumption were assessed in 642 participants from the Baltimore Longitudinal Study of Aging. Results indicate that personality traits were mostly unrelated to resting metabolic rate and energy expenditure at normal walking pace. However, those who scored lower on neuroticism (r =  −0.12) and higher on extraversion (r = 0.11), openness (r = 0.13), and conscientiousness (r = 0.09) had significantly higher energy expenditure at peak walking pace. In addition to greater aerobic capacity, individuals with a more resilient personality profile walked faster and were more efficient in that they required less energy per meter walked. The associations between personality and energy expenditure were not moderated by age or sex, but were in part explained by the proportion of fat mass. In conclusion, differences in personality may matter the most during more challenging activities that require cardiorespiratory fitness. These findings suggest potential pathways that link personality to health outcomes, such as obesity and longevity.     

Do drivers intentionally target wildlife on roads?

Despite frequent reliance on surveys to document public attitudes towards conservation issues (such as invasive‐species control), only rarely do researchers assess the validity of statements made by the public in response to such surveys. Therefore, how well responses match actual behaviour remains an open question. We conducted a survey asking drivers if they had seen and/or run over (intentionally or not) snakes, native frogs or invasive cane toads (Rhinella marina) on roads in the Northern Territory of Australia. To compare actual driver behaviour to the survey responses, we also carried out field experiments where we quantified the rates at which model snakes, frogs and toads (and controls) were run over on a rural highway. Our results show a discrepancy between survey responses and driver behaviour: for example, 25% of the people we surveyed indicated that they intentionally run over cane toads, yet field experiments showed that model toads were run over no more frequently than expected by chance, or than any other type of model.     

Male Weasels Decrease Activity and Energy Expenditure in Response to High Ambient Temperatures

The heat dissipation limit (HDL) hypothesis suggests that the capacity of endotherms to dissipate body heat may impose constraints on their energy expenditure. Specifically, this hypothesis predicts that endotherms should avoid the detrimental consequences of hyperthermia by lowering their energy expenditure and reducing their activity in response to high ambient temperatures (T_a). We used an extensive data set on the daily energy expenditure (DEE, n = 27) and the daily activity time (AT, n = 48) of male weasels (Mustela nivalis) during the spring and summer breeding season to test these predictions. We found that T_a was related in a “hump-shaped” (i.e. convex) manner to AT, DEE, resting metabolic rate (RMR) and metabolic scope (the ratio of DEE to RMR). These results support the HDL hypothesis because in response to warm T_as male weasels reduced their AT, DEE, and RMR. Although the activity and energy expenditure of large endotherms are most likely to be constrained in response to warm T_as because they are less able to dissipate heat, our results suggest that small endotherms may also experience constraints consistent with the HDL hypothesis.     

Use of overall dynamic body acceleration for estimating energy expenditure in cormorants: Does locomotion in different media affect relationships?

The way in which animals use and acquire energy is fundamental to their fitness. Overall dynamic body acceleration (ODBA) has recently been suggested as a new method for the determination of energy expenditure in wild animals. Although the relationship between ODBA and energy expenditure has been calibrated using gas-respirometry, it has only been validated for animals moving in a single medium. In this work we examined whether the relationship between ODBA and energy expenditure varies between activity types and in particular, how locomotion in different media affects the regressions using the Imperial Cormorant Phalacrocorax atriceps as a model species. Regressing mean ODBA values for resting, diving and walking periods on a single graph against mean power values, the mass-specific power (W kg⁻¹) was related to ODBA via; Power = 12.09 + 41.31 ODBA (r² = 0.93). Although values for resting, walking and swimming all fell close to a single linear fit, values for flight deviated substantially from this. The different relationships found between locomotory types are discussed in terms of the muscle groups involved in each kind of behavior.     

The covariance between metabolic rate and behaviour varies across behaviours and thermal types: meta‐analytic insights

Energy metabolism has received much attention as a potential driver of repeatable among‐individual differences in behaviour (animal personality). Several factors have been hypothesized to mediate this relationship. We performed a systematic review with a meta‐analysis of >70 studies comprised of >8000 individuals reporting relationships between measures of maintenance metabolic rates (i.e. basal metabolic rate, resting metabolic rate, and standard metabolic rate) and behaviour. We evaluated support for three hypothesized mediators: (i) type of behaviour, (ii) opportunities for energy re‐allocation, and (iii) magnitude of energetic constraints. Relationships between measures of maintenance metabolic rate (MR) and behaviour are predicted to be strongest for behaviours with strong consequences for energy turnover (acquisition or expenditure). Consistent with this, we found that behaviours with known consequences for energy gain (e.g. foraging, dominance, boldness) or expenditure (e.g. maximum sprint speed, sustained running speed, maximum distance travelled, etc.) had strong positive correlations with MR, while behaviours with putatively weak and/or inconsistent associations with net energy gain or loss (e.g. exploration, activity, sociability) were not correlated with MR. Greater opportunities for energy reallocation are predicted to weaken relationships between MR and behaviour by creating alternative pathways to balance energy budgets. We tested this by contrasting relationships between MR and behaviour in ectotherms versus endotherms, as thermoregulation in endotherms creates additional opportunities for energy reallocation compared with ectotherms. As predicted, the relationship between behaviour and MR was stronger in ectotherms compared with endotherms. However, statistical analyses of heterogeneity among effect sizes from different species did not support energy re‐allocation as the main driver of these differences. Finally, we tested whether conditions where animals face greater constraints in meeting their energy budgets (e.g. field versus laboratory, breeding versus non‐breeding) increased the strength of the relationship between MR and behaviour. We found that the relationship between MR and behaviour was unaffected by either of these modifiers. This meta‐analysis provides two key insights. First, we observed positive relationships of similar magnitude between MR and behaviours that bring in net energy, and behaviours that cost net energy. This result is only consistent with a performance energy‐management model. Given that the studies included in our meta‐analysis represent a wide range of taxa, this suggests that the performance model may be the most common model in general. Second, we found that behaviours with putatively weak or inconsistent consequences for net energy gain or expenditure (exploration, activity, sociability) show no relationship with MR. The lack of relationship between MR and behavioural traits with weak and/or inconsistent consequences for energy turnover provides the first systematic demonstration of the central importance of the ecological function of traits in mediating relationships between MR and behaviour.     

Not such silly sausages: Evidence suggests northern quolls exhibit aversion to toads after training with toad sausages

The invasion of toxic cane toads (Rhinella marina) is a major threat to northern quolls (Dasyurus hallucatus) which are poisoned when they attack this novel prey item. Quolls are now endangered as a consequence of the toad invasion. Conditioned taste aversion can be used to train individual quolls to avoid toads, but we currently lack a training technique that can be used at a landscape scale to buffer entire populations from toad impact. Broad‐scale deployment requires a bait that can be used for training, but there is no guarantee that such a bait will ultimately elicit aversion to toads. Here, we test a manufactured bait – a ‘toad sausage’ – in a small captive trial, for its ability to elicit aversion to toads in northern quolls. To do this, we exposed one group of quolls to a toad sausage and another to a control sausage and compared the quolls' predatory responses when presented with a dead adult toad. Captive quolls that consumed a single toad sausage showed a reduced interest in cane toads, interacting with them for less than half the time of their untrained counterparts and showing reduced Attack behaviour. We also quantified bait uptake in the field, by both quolls and non‐target species. These field trials showed that wild quolls were the most frequent species attracted to the baits, and that approx. 61% of quolls consumed toad‐aversion baits when first encountered. Between 40% and 68% of these animals developed aversion to further bait consumption. Our results suggest that toad‐aversion sausages may be used to train wild quolls to avoid cane toads. This opens the possibility for broad‐scale quoll training with toad aversion sausages: a technique that may allow wildlife managers to prevent quoll extinctions at a landscape scale.     

Skin resistance to water gain and loss has changed in cane toads (Rhinella marina) during their Australian invasion

The water‐permeable skin of amphibians renders them highly sensitive to climatic conditions, and interspecific correlations between environmental moisture levels and rates of water exchange across the skin suggest that natural selection adapts hydroregulatory mechanisms to local challenges. How quickly can such mechanisms shift when a species encounters novel moisture regimes? Cutaneous resistance to water loss and gain in wild‐caught cane toads (Rhinella marina) from Brazil, USA (Hawai''i) and Australia exhibited strong geographic variation. Cutaneous resistance was low in native‐range (Brazilian) toads and in Hawai''ian populations (where toads were introduced in 1932) but significantly higher in toads from eastern Australia (where toads were introduced in 1935). Toads from recently invaded areas in western Australia exhibited cutaneous resistance to water loss similar to the native‐range populations, possibly because toads are restricted to moist sites within this highly arid landscape. Rates of rehydration exhibited significant but less extreme geographic variation, being higher in the native range than in invaded regions. Thus, in less than a century, cane toads invading areas that impose different climatic challenges have diverged in the capacity for hydroregulation.     

Behavioural tactics used by invasive cane toads (Rhinella marina) to exploit apiaries in Australia

Behavioural flexibility plays a key role in facilitating the ability of invasive species to exploit anthropogenically‐created resources. In Australia, invasive cane toads (Rhinella marina) often gather around commercial beehives (apiaries), whereas native frogs do not. To document how toads use this resource, we spool‐tracked cane toads in areas containing beehives and in adjacent natural habitat without beehives, conducted standardized observations of toad feeding behaviour, and ran prey‐manipulation trials to compare the responses of cane toads versus native frogs to honeybees as potential prey. Toads feeding around beehives travelled shorter distances per night, and hence used different microhabitats, than did toads from nearby control sites without beehives. The toads consumed live bees from the hive entrance (rather than dead bees from the ground), often climbing on top of one another to gain access to the hive entrance. Prey manipulation trials confirm that bee movement is the critical stimulus that elicits the toads’ feeding response; and in standardized trials, native frogs consumed bees less frequently than did toads. In summary, cane toads flexibly modify their movements, foraging behaviour and dietary composition to exploit the nutritional opportunities created by commercial beehives, whereas native anurans do not.